The role of the Syk/Shp-1 kinase-phosphatase equilibrium in B cell development and signaling

Journal of Immunology

Volumn 193, Issue 1, 2014, Pages 268-276

  Alsadeq, Ameera ^a,b   Hobeika, Elias ^a,b   Medgyesi, David ^a,b   Kläsener, Kathrin ^a,b   Reth, Michael ^a,b  

^a MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD40 ANTIGEN; CD86 ANTIGEN; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A; IMMUNOGLOBULIN G2B; IMMUNOGLOBULIN G3; PROTEIN KINASE SYK; PROTEIN KINASE ZAP 70; PROTEIN TYROSINE PHOSPHATASE SHP 1; TOLL LIKE RECEPTOR;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; CALCIUM CELL LEVEL; CALCIUM MOBILIZATION; CELL MATURATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME LOCALIZATION; EX VIVO STUDY; HOMEOSTASIS; IMMUNOGLOBULIN BLOOD LEVEL; LYMPHOCYTE COUNT; LYMPHOCYTE FUNCTION; LYMPHOCYTE PROLIFERATION; LYMPHOCYTE SUBPOPULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; B-LYMPHOCYTE SUBSETS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, KNOCKOUT; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 6; PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION; ZAP-70 PROTEIN-TYROSINE KINASE;

EID: 84903625195     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1203040     Document Type: Article

References (69)

1. Fugmann, S. D., A. I. Lee, P. E. Shockett, I. J. Villey, and D. G. Schatz. 2000. The RAG proteins and V(D)J recombination: complexes, ends, and transposition. Annu. Rev. Immunol. 18: 495-527.
2. Hardy, R. R., Y. S. Li, D. Allman, M. Asano, M. Gui, and K. Hayakawa. 2000. B-cell commitment, development and selection. Immunol. Rev. 175: 23-32.
3. Rolink, A. G., C. Schaniel, J. Andersson, and F. Melchers. 2001. Selection events operating at various stages in B cell development. Curr. Opin. Immunol. 13: 202-207.
4. Hardy, R. R., and K. Hayakawa. 2001. B cell development pathways. Annu. Rev. Immunol. 19: 595-621.
5. Herzenberg, L. A., and J. W. Tung. 2006. B cell lineages: documented at last! Nat. Immunol. 7: 225-226.
6. Berland, R., and H. H. Wortis. 2002. Origins and functions of B-1 cells with notes on the role of CD5. Annu. Rev. Immunol. 20: 253-300.
7. Reth, M., and J. Wienands. 1997. Initiation and processing of signals from the B cell antigen receptor. Annu. Rev. Immunol. 15: 453-479.
8. Reth, M. 1995. The B-cell antigen receptor complex and co-receptors. Immunol. Today 16: 310-313.
9. Kurosaki, T. 1999. Genetic analysis of B cell antigen receptor signaling. Annu. Rev. Immunol. 17: 555-592.
10. Geahlen, R. L. 2009. Syk and pTyr'd: Signaling through the B cell antigen receptor. Biochim. Biophys. Acta 1793: 1115-1127.
11. Kurosaki, T., and M. Hikida. 2009. Tyrosine kinases and their substrates in B lymphocytes. Immunol. Rev. 228: 132-148.
12. Kraus, M., L. I. Pao, A. Reichlin, Y. Hu, B. Canono, J. C. Cambier, M. C. Nussenzweig, and K. Rajewsky. 2001. Interference with immunoglobulin (Ig)alpha immunoreceptor tyrosine-based activation motif (ITAM) phosphorylation modulates or blocks B cell development, depending on the availability of an Igbeta cytoplasmic tail. J. Exp. Med. 194: 455-469.
13. Rolli, V., M. Gallwitz, T. Wossning, A. Flemming, W. W. Schamel, C. Zürn, and M. Reth. 2002. Amplification of B cell antigen receptor signaling by a Syk/ITAM positive feedback loop. Mol. Cell 10: 1057-1069.
14. Werner, M., E. Hobeika, and H. Jumaa. 2010. Role of PI3K in the generation and survival of B cells. Immunol. Rev. 237: 55-71.
15. Aiba, Y., M. Kameyama, T. Yamazaki, T. F. Tedder, and T. Kurosaki. 2008. Regulation of B-cell development by BCAP and CD19 through their binding to phosphoinositide 3-kinase. Blood 111: 1497-1503.
16. Kurosaki, T., and S. Tsukada. 2000. BLNK: connecting Syk and Btk to calcium signals. Immunity 12: 1-5.
17. Takata, M., H. Sabe, A. Hata, T. Inazu, Y. Homma, T. Nukada, H. Yamamura, and T. Kurosaki. 1994. Tyrosine kinases Lyn and Syk regulate B cell receptorcoupled Ca2+ mobilization through distinct pathways. EMBO J. 13: 1341-1349.
18. Kulathu, Y., E. Hobeika, G. Turchinovich, and M. Reth. 2008. The kinase Syk as an adaptor controlling sustained calcium signalling and B-cell development. EMBO J. 27: 1333-1344.
19. Jiang, A., A. Craxton, T. Kurosaki, and E. A. Clark. 1998. Different protein tyrosine kinases are required for B cell antigen receptor-mediated activation of extracellular signal-regulated kinase, c-Jun NH2-terminal kinase 1, and p38 mitogen-activated protein kinase. J. Exp. Med. 188: 1297-1306.
20. Cornall, R. J., A. M. Cheng, T. Pawson, and C. C. Goodnow. 2000. Role of Syk in B-cell development and antigen-receptor signaling. Proc. Natl. Acad. Sci. USA 97: 1713-1718.
21. Cheng, A. M., B. Rowley, W. Pao, A. Hayday, J. B. Bolen, and T. Pawson. 1995. Syk tyrosine kinase required for mouse viability and B-cell development. Nature 378: 303-306.
22. Turner, M., P. J. Mee, P. S. Costello, O. Williams, A. A. Price, L. P. Duddy, M. T. Furlong, R. L. Geahlen, and V. L. Tybulewicz. 1995. Perinatal lethality and blocked B-cell development in mice lacking the tyrosine kinase Syk. Nature 378: 298-302.
23. Turner, M., A. Gulbranson-Judge, M. E. Quinn, A. E. Walters, I. C. MacLennan, and V. L. Tybulewicz. 1997. Syk tyrosine kinase is required for the positive selection of immature B cells into the recirculating B cell pool. J. Exp. Med. 186: 2013-2021.
24. Cornall, R. J., J. G. Cyster, M. L. Hibbs, A. R. Dunn, K. L. Otipoby, E. A. Clark, and C. C. Goodnow. 1998. Polygenic autoimmune traits: Lyn, CD22, and SHP-1 are limiting elements of a biochemical pathway regulating BCR signaling and selection. Immunity 8: 497-508.
25. Zikherman, J., K. Doan, R. Parameswaran, W. Raschke, and A. Weiss. 2012. Quantitative differences in CD45 expression unmask functions for CD45 in B-cell development, tolerance, and survival. Proc. Natl. Acad. Sci. USA 109: E3-E12.
26. Zhu, J. W., T. Brdicka, T. R. Katsumoto, J. Lin, and A. Weiss. 2008. Structurally distinct phosphatases CD45 and CD148 both regulate B cell and macrophage immunoreceptor signaling. Immunity 28: 183-196.
27. Pao, L. I., K. Badour, K. A. Siminovitch, and B. G. Neel. 2007. Nonreceptor protein-tyrosine phosphatases in immune cell signaling. Annu. Rev. Immunol. 25: 473-523.
28. Neel, B. G. 1997. Role of phosphatases in lymphocyte activation. Curr. Opin. Immunol. 9: 405-420.
29. Shultz, L. D., P. A. Schweitzer, T. V. Rajan, T. Yi, J. N. Ihle, R. J. Matthews, M. L. Thomas, and D. R. Beier. 1993. Mutations at the murine motheaten locus are within the hematopoietic cell protein-tyrosine phosphatase (Hcph) gene. Cell 73: 1445-1454.
30. Tsui, H. W., K. A. Siminovitch, L. de Souza, and F. W. Tsui. 1993. Motheaten and viable motheaten mice have mutations in the haematopoietic cell phosphatase gene. Nat. Genet. 4: 124-129.
31. Shultz, L. D., D. R. Coman, C. L. Bailey, W. G. Beamer, and C. L. Sidman. 1984. "Viable motheaten," a new allele at the motheaten locus. I. Pathology. Am. J. Pathol. 116: 179-192.
32. Shultz, L. D. 1988. Pleiotropic effects of deleterious alleles at the "motheaten" locus. Curr. Top. Microbiol. Immunol. 137: 216-222.
33. Hayes, S. M., L. D. Shultz, and D. L. Greiner. 1992. Thymic involution in viable motheaten (me(v)) mice is associated with a loss of intrathymic precursor activity. Dev. Immunol. 2: 191-205.
34. Davidson, W. F., H. C. Morse, III, S. O. Sharrow, and T. M. Chused. 1979. Phenotypic and functional effects of the motheaten gene on murine B and T lymphocytes. J. Immunol. 122: 884-891.
35. Sidman, C. L., L. D. Shultz, and E. R. Unanue. 1978. The mouse mutant "motheaten." II. Functional studies of the immune system. J. Immunol. 121: 2399-2404.
36. Pao, L. I., K.-P. Lam, J. M. Henderson, J. L. Kutok, M. Alimzhanov, L. Nitschke, M. L. Thomas, B. G. Neel, and K. Rajewsky. 2007. B cell-specific deletion of protein-tyrosine phosphatase Shp1 promotes B-1a cell development and causes systemic autoimmunity. Immunity 27: 35-48.
37. Dustin, L. B., D. R. Plas, J. Wong, Y. T. Hu, C. Soto, A. C. Chan, and M. L. Thomas. 1999. Expression of dominant-negative src-homology domain 2-containing protein tyrosine phosphatase-1 results in increased Syk tyrosine kinase activity and B cell activation. J. Immunol. 162: 2717-2724.
38. Cyster, J. G., and C. C. Goodnow. 1995. Protein tyrosine phosphatase 1C negatively regulates antigen receptor signaling in B lymphocytes and determines thresholds for negative selection. Immunity 2: 13-24.
39. Adachi, T., J. Wienands, C. Wakabayashi, H. Yakura, M. Reth, and T. Tsubata. 2001. SHP-1 requires inhibitory co-receptors to down-modulate B cell antigen receptor-mediated phosphorylation of cellular substrates. J. Biol. Chem. 276: 26648-26655.
40. Saijo, K., C. Schmedt, I. H. Su, H. Karasuyama, C. A. Lowell, M. Reth, T. Adachi, A. Patke, A. Santana, and A. Tarakhovsky. 2003. Essential role of Src-family protein tyrosine kinases in NF-kappaB activation during B cell development. Nat. Immunol. 4: 274-279.
41. Hobeika, E., S. Thiemann, B. Storch, H. Jumaa, P. J. Nielsen, R. Pelanda, and M. Reth. 2006. Testing gene function early in the B cell lineage in mb1-cre mice. Proc. Natl. Acad. Sci. USA 103: 13789-13794.
42. Jumaa, H., G. Wei, and P. J. Nielsen. 1999. Blastocyst formation is blocked in mouse embryos lacking the splicing factor SRp20. Curr. Biol. CB 9: 899-902.
43. Hardy, R. R., C. E. Carmack, S. A. Shinton, J. D. Kemp, and K. Hayakawa. 1991. Resolution and characterization of pro-B and pre-pro-B cell stages in normal mouse bone marrow. J. Exp. Med. 173: 1213-1225.
44. Minguet, S., E. P. Dopfer, C. Pollmer, M. A. Freudenberg, C. Galanos, M. Reth, M. Huber, and W. W. Schamel. 2008. Enhanced B-cell activation mediated by TLR4 and BCR crosstalk. Eur. J. Immunol. 38: 2475-2487.
45. Roes, J., and K. Rajewsky. 1993. Immunoglobulin D (IgD)-deficient mice reveal an auxiliary receptor function for IgD in antigen-mediated recruitment of B cells. J. Exp. Med. 177: 45-55.
46. Söderberg, O., K. J. Leuchowius, M. Gullberg, M. Jarvius, I. Weibrecht, L. G. Larsson, and U. Landegren. 2008. Characterizing proteins and their interactions in cells and tissues using the in situ proximity ligation assay. Methods 45: 227-232.
47. Marshall-Clarke, S., L. Tasker, M. P. Heaton, and R. M. Parkhouse. 2003. A differential requirement for phosphoinositide 3-kinase reveals two pathways for inducible upregulation of major histocompatibility complex class II molecules and CD86 expression by murine B lymphocytes. Immunology 109: 102-108.
48. Schweighoffer, E., L. Vanes, A. Mathiot, T. Nakamura, and V. L. J. Tybulewicz. 2003. Unexpected requirement for ZAP-70 in pre-B cell development and allelic exclusion. Immunity 18: 523-533.
49. Infantino, S., B. Benz, T. Waldmann, M. Jung, R. Schneider, and M. Reth. 2010. Arginine methylation of the B cell antigen receptor promotes differentiation. J. Exp. Med. 207: 711-719.
50. Königsberger, S., J. Prodöhl, D. Stegner, V. Weis, M. Andreas, M. Stehling, T. Schumacher, R. Böhmer, I. Thielmann, J. M. van Eeuwijk, et al. 2012. Altered BCR signalling quality predisposes to autoimmune disease and a pre-diabetic state. EMBO J. 31: 3363-3374.
51. Heng, T. S., M. W. Painter; Immunological Genome Project Consortium. 2008. The Immunological Genome Project: networks of gene expression in immune cells. Nat. Immunol. 9: 1091-1094.
52. Su, Y. W., and H. Jumaa. 2003. LAT links the pre-BCR to calcium signaling. Immunity 19: 295-305.
53. Oya, K., J. Wang, Y. Watanabe, R. Koga, and T. Watanabe. 2003. Appearance of the LAT protein at an early stage of B-cell development and its possible role. Immunology 109: 351-359.
54. Fallah-Arani, F., E. Schweighoffer, L. Vanes, and V. L. J. Tybulewicz. 2008. Redundant role for Zap70 in B cell development and activation. Eur. J. Immunol. 38: 1721-1733.
55. Plas, D. R., R. Johnson, J. T. Pingel, R. J. Matthews, M. Dalton, G. Roy, A. C. Chan, and M. L. Thomas. 1996. Direct regulation of ZAP-70 by SHP-1 in T cell antigen receptor signaling. Science 272: 1173-1176.
56. Raab, M., and C. E. Rudd. 1996. Hematopoietic cell phosphatase (HCP) regulates p56LCK phosphorylation and ZAP-70 binding to T cell receptor zeta chain. Biochem. Biophys. Res. Commun. 222: 50-57.
57. Kosugi, A., J. Sakakura, K. Yasuda, M. Ogata, and T. Hamaoka. 2001. Involvement of SHP-1 tyrosine phosphatase in TCR-mediated signaling pathways in lipid rafts. Immunity 14: 669-680.
58. Jin, Y. J., C. L. Yu, and S. J. Burakoff. 1999. Human 70-kDa SHP-1L differs from 68-kDa SHP-1 in its C-terminal structure and catalytic activity. J. Biol. Chem. 274: 28301-28307.
59. Kon-Kozlowski, M., G. Pani, T. Pawson, and K. A. Siminovitch. 1996. The tyrosine phosphatase PTP1C associates with Vav, Grb2, and mSos1 in hematopoietic cells. J. Biol. Chem. 271: 3856-3862.
60. Kawasaki, N., C. Rademacher, and J. C. Paulson. 2011. CD22 regulates adaptive and innate immune responses of B cells. J. Innate Immun. 3: 411-419.
61. Sato, S., A. S. Miller, M. Inaoki, C. B. Bock, P. J. Jansen, M. L. Tang, and T. F. Tedder. 1996. CD22 is both a positive and negative regulator of B lymphocyte antigen receptor signal transduction: altered signaling in CD22-deficient mice. Immunity 5: 551-562.
62. Mora, J. R., M. Iwata, B. Eksteen, S. Y. Song, T. Junt, B. Senman, K. L. Otipoby, A. Yokota, H. Takeuchi, P. Ricciardi-Castagnoli, et al. 2006. Generation of guthoming IgA-secreting B cells by intestinal dendritic cells. Science 314: 1157-1160.
63. Cerutti, A. 2008. The regulation of IgA class switching. Nat. Rev. Immunol. 8: 421-434.
64. Cerutti, A., and M. Rescigno. 2008. The biology of intestinal immunoglobulin A responses. Immunity 28: 740-750.
65. Hoffmann, A., S. Kerr, J. Jellusova, J. Zhang, F. Weisel, U. Wellmann, T. H. Winkler, B. Kneitz, P. R. Crocker, and L. Nitschke. 2007. Siglec-G is a B1 cell-inhibitory receptor that controls expansion and calcium signaling of the B1 cell population. Nat. Immunol. 8: 695-704.
66. Jellusova, J., U. Wellmann, K. Amann, T. H. Winkler, and L. Nitschke. 2010. CD22 x Siglec-G double-deficient mice have massively increased B1 cell numbers and develop systemic autoimmunity. J. Immunol. 184: 3618-3627.
67. Schweighoffer, E., L. Vanes, J. Nys, D. Cantrell, S. McCleary, N. Smithers, and V. L. Tybulewicz. 2013. The BAFF receptor transduces survival signals by coopting the B cell receptor signaling pathway. Immunity 38: 475-488.
68. Wheeler, M. L., and A. L. Defranco. 2012. Prolonged production of reactive oxygen species in response to B cell receptor stimulation promotes B cell activation and proliferation. J. Immunol. 189: 4405-4416.
69. Reth, M. 2002. Hydrogen peroxide as second messenger in lymphocyte activation. Nat. Immunol. 3: 1129-1134.